The Patterns and Causes of Dermatitis in Terrestrial and Semi-Aquatic Mammalian Wildlife

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Review
The Patterns and Causes of Dermatitis in Terrestrial and
Semi-Aquatic Mammalian Wildlife
Elise M. Ringwaldt * , Barry W. Brook                     , Scott Carver        and Jessie C. Buettel

                                          School of Natural Sciences, University of Tasmania, Hobart, TAS 7000, Australia;
                                          Barry.Brook@utas.edu.au (B.W.B.); Scott.Carver@utas.edu.au (S.C.); Jessie.Buettel@utas.edu.au (J.C.B.)
                                          * Correspondence: Elise.Ringwaldt@utas.edu.au

                                          Simple Summary: Dermatitis is recognized to manifest from a variety of causes in humans and
                                          animals, but these have never been synthesized for wildlife. We document the causes and investigate
                                          the magnitude of skin diseases and disorders which manifest as, and are described as, dermatitis
                                          in the published literature. Our aim was to identify the major causal agents in the development
                                          of dermatitis, and if certain mammalian wildlife groups or captivity status was a precursor for
                                          the development of dermatitis. The most common causes of dermatitis identified were mites,
                                          bacteria, and fungus, and were more frequently reported for wildlife species within Carnivora and
                                          Artiodactyla. Furthermore, associated with genetic and behavioral variables, some threatened species
                                          were more likely to exhibit dermatitis in captivity. This study provides insight into wild mammalian
                                          species that may be more susceptible to dermatological diseases and discusses the patterns of causes
                                          within wild mammals.

                                Abstract: Causative disease and stress agents which manifest as dermatitis in mammals have varying
         
                                          effects on individual animals, from benign irritation and inflammation, to causing morbidity and
Citation: Ringwaldt, E.M.; Brook,         even mortality. Bacteria, viruses and ectoparasites are all potential causes of dermatitis, and it can
B.W.; Carver, S.; Buettel, J.C. The
                                          be exacerbated by various environmental, genetic and social factors. Furthermore, it is uncertain
Patterns and Causes of Dermatitis in
                                          whether dermatitis is more likely to manifest in already-vulnerable wildlife species. Here, we
Terrestrial and Semi-Aquatic
                                          systematically review the literature for reports of dermatitis in terrestrial and semi-aquatic wild
Mammalian Wildlife. Animals 2021,
                                          mammalian species, with the goal of determining the biogeographical scale of dermatitis reports, the
11, 1691. https://doi.org/10.3390/
ani11061691
                                          causes of dermatitis, and whether manifestation of dermatitis is reported more commonly in certain
                                          wildlife species or their captivity status (i.e., free-living, in captivity or in a laboratory). We reveal
Academic Editor: Nicole Gottdenker        biases in the reporting of dermatitis by a biogeographic realm, with 55% of cases reported in the
                                          Nearctic, and towards particular orders of mammals, namely Artiodactyla and Carnivora. Overall,
Received: 17 May 2021                     free-living wildlife is almost twice as likely to be reported as having dermatitis than individuals in
Accepted: 3 June 2021                     captivity and six times more likely than individuals in laboratories, which we interpret as owing
Published: 6 June 2021                    to exposure to a broader spectrum of parasites in free-ranging individuals, and potential reporting
                                          bias in captive individuals. Notably, dermatitis was reported in 23 threatened species, with some
Publisher’s Note: MDPI stays neutral      species more likely than others to be reported exhibiting clinical signs of dermatitis resulting from
with regard to jurisdictional claims in
                                          underlying health problems. We also find that threatened species are more likely to be reported
published maps and institutional affil-
                                          as having dermatitis in captivity, particularly outside of their endemic home range. This review
iations.
                                          highlights diverse patterns of dermatological disease causes in captive and free-ranging wildlife,
                                          conditions under which they are more likely to be documented, and the need for cross-disciplinary
                                          research to ascertain (and so better manage) the varied causes.

Copyright: © 2021 by the authors.
                                          Keywords: captivity; dermatitis; dermatophilosis; exudative dermatitis; free-living; mammal; threat-
Licensee MDPI, Basel, Switzerland.
                                          ened species; wildlife
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).

Animals 2021, 11, 1691. https://doi.org/10.3390/ani11061691                                                   https://www.mdpi.com/journal/animals
Animals 2021, 11, 1691                                                                                              2 of 19

                         1. Introduction
                               Dermatitis is a general term for describing different forms of skin irritation and
                         inflammation in humans and animals, with some causes of dermatitis being zoonotic and
                         transmissible between people, domestic or captive animals and wildlife [1,2]. Dermatitis
                         in humans and animals has been associated with reduced quality of life [3,4] and reports
                         of dermatitis in threatened species indicates that skin diseases can also be a threat to
                         persistence [5]. Dermatitis is the term for inflammation of the skin, which can have
                         many different possible causes [2]. The development of clinical signs of dermatitis can be
                         due to health issues such as infectious agents, ectoparasites, environmental irritants, or
                         unknown [6,7]. Research into the cause and treatment of dermatitis has focused on either
                         human health (e.g., [8,9]), or domestic animals and livestock (e.g., [10]). For some wildlife
                         species, including many of conservation concern, the etiological agent or mechanisms
                         behind dermatitis origins are unclear (e.g., [11,12]). The etiological agents which can trigger
                         dermatitis may cause different effects in individuals; however, the question of whether
                         there are patterns to the formation of dermatitis clinical signs for diseases or irritants across
                         wildlife has yet to be determined.
                               Clinically, there are different types of dermatitis that can be detected by physical
                         examination, sampling techniques (e.g., skin swabbing, skin scrapings, UV light), or may
                         require histological examination of tissues [13]. Following detection of dermal lesions, a
                         common challenge is identifying the causal agent(s). This is because the causes of dermatitis
                         are variable and can also be species specific, for instance, grey squirrels (Sciurus carolinensis)
                         do not display clinical signs to the parapoxvirus but spread it to red squirrels (Sciurus
                         vulgaris) where it, by contrast, causes exudative dermatological lesions [12,14]. Even within
                         the same species, dermatitis can manifest in a range of ways, from benign, moderate (e.g.,
                         hair loss), to severe (e.g., ulcerative pustules and necrosis) and mortality causing [5,15].
                         Benign dermatitis lesions can also lead to secondary infections through self-trauma or
                         exposure to opportunistic pathogens [16–18].
                               Historically, research has primarily focused on wildlife exhibiting dermatitis acting as
                         reservoirs for the pathogen, potentially spilling over into livestock and causing economic
                         losses in agriculture animals, or transmission to humans due to proximity [1,2,10,19].
                         However, more recently, due to the increasing recognition of the role of infectious disease
                         in the modern biodiversity crisis, some skin diseases, with dermatitis as an important
                         clinical sign, such as Sarcoptic mange and White Nose Syndrome, have been viewed as
                         an additional conservation pressure on already-threatened species [20–23]. Furthermore,
                         it is unclear if there are generalities to the onset and progression of the clinical signs of
                         dermatitis as a manifestation of skin disease across taxa.
                               The occurrence of dermatitis in wildlife species is global, and, from an animal ethics
                         perspective, morbidity and mortality from secondary skin infections can be an incontro-
                         vertible wildlife management issue [10,24]. Dermatitis has been reported in mammalian
                         wildlife which are already of conservation concern (e.g., [25–27]) and in some cases animals
                         have died with severe dermatitis or secondary infections [28]. Within the last 10 years,
                         the specific term ‘exudative dermatitis’ has been used as a common descriptive symptom
                         in wildlife reports (e.g., [12,29]) and is a type of emerging dermatitis in some Australian
                         wildlife [30,31]. Therefore, investigating whether specific types of mammalian wildlife are
                         more likely to be reported as showing dermatitis as a manifestation of disease, and due to
                         which causal agent, may aid in understanding skin disease risks.
                               In this review, we aim to consolidate the literature of terrestrial and semi-aquatic
                         mammalian wildlife that are reported to exhibit dermatitis: firstly, to explore whether
                         reports of dermatitis are more likely for types of etiological agents; and, secondly, whether
                         documentation of dermatitis is similar across mammalian wildlife groups or reported more
                         often in some orders. Additionally, we also identify biases in the reporting of dermatitis,
                         and investigate threatened species reported as suffering from dermatitis as an added
                         pressure for species already subjected to environmental and anthropogenic threats. We
                         attempt to be exhaustive in our search of published reports of dermatitis in the literature,
Animals 2021, 11, 1691                                                                                                3 of 19

                         and results herein broadly align with general perceptions across a range of texts and sources.
                         We recognize not all cases fitting the definition are always explicitly termed ‘dermatitis’ in
                         wildlife, and thus do not claim this review to cover every possible study encompassing
                         dermatitis symptoms (which we discuss), but we have reasons to be confident that this
                         review captures general patterns and is thus an appropriate synthesis contributing a general
                         understanding of this condition in wildlife.

                         2. Database Search and Literature Screening
                               To identify the relevant literature, we searched three databases in December 2019 and
                         additionally in March 2021: Web of Science, Scopus and Google Scholar using the search
                         string in the topic of: title, abstract and key words, ‘“dermatitis” OR “exudative dermatitis”
                         AND “wildlife”’ (Search terms S1). We imported all records from Web of Science and
                         Scopus, and the first-100 papers (ranked-by-relevance) were exported from Google Scholar
                         for screening to reduce disparate articles (Figure 1). We restricted our literature review
                         to peer-reviewed publications—as the most robust and defendable source of reports—
                         available in these most widely used and publicly available databases to researchers. We
                         acknowledge that this will preclude some non-journal literature (e.g., annual reports,
                         conference proceedings, books) available in less widely available databases, such as CAB,
                         which may contain additional reports that could be considered in future analyses.
                               After duplicate articles were removed, articles were first screened by title and abstract
                         for relevance to dermatitis and wildlife and those not meeting the inclusion criteria were
                         removed (Figure 1). We then assessed the full text of the filtered list of articles to identify
                         records that fit our eligibility criteria. We only included articles which described anywhere
                         in text, signs of histopathological or superficial dermatitis affecting the mammal in question.
                         To ensure comprehensiveness of the literature search, we also screened the bibliographies
                         and reference lists from the final full-text articles (Figure 1).

                         2.1. Inclusion and Exclusion Criteria
                              All articles were included in this review if they focused on wild (terrestrial or semi-
                         aquatic) mammals that reported physical lesions that were diagnosed as dermatitis (re-
                         gardless of the cause). Articles in this review only included records of mammals exhibiting
                         dermatological clinical signs, and, therefore, manuscripts which focused exclusively on
                         serological surveys of pathogens/antibodies which may cause dermatitis were excluded.
                         Articles were also excluded if the focus of the research was a review, conference proceed-
                         ings, or book review. After the screening process, articles were also excluded if they only
                         used data from a previously published study.

                         2.2. Data Extraction
                              For each article, we extracted numeric, categorical, and written information about
                         the manuscript, mammal species exhibiting dermatitis, and the agent causing dermatitis
                         (Table 1; Table S2).

                         Table 1. Article Data Extraction: for each article, we collected information on the manuscript, the
                         individuals per species, and the dermatitis exhibited by each species.

                                   Manuscript                    Mammal (Per Species)          Dermatitis (Per Species)
                                       Title                     Number of individuals                  Type
                                    Author(s)                      Captivity status             Location of dermatitis
                                       Year                            Country                      Clinical signs
                                     Journal                      Conservation status             Definitive Cause
                                    Key terms
Animals 2021, 11, 1691                                                                                                                  4 of 19
Animals 2021, 11, x                                                                                                                     4 of 20

      Figure 1. Protocol for screening articles after data base search of “dermatitis” OR “exudative dermatitis” AND “wildlife”.
                                                                                                                     “wildlife”.
      Each step shows  the number   of papers  included   or excluded for review.
      Each step shows the number of papers included or excluded for review.

                                       For articles
                                       After         witharticles
                                              duplicate     multiplewere species,   we recorded
                                                                              removed,      articlesdata
                                                                                                     wereforfirst
                                                                                                               all individuals
                                                                                                                    screened byexhibiting
                                                                                                                                     title and
                                 signs of dermatitis.
                                 abstract  for relevance When     more than and
                                                             to dermatitis       one species
                                                                                      wildlifeofand
                                                                                                  mammal
                                                                                                      those was     studied, we
                                                                                                              not meeting      the separated
                                                                                                                                    inclusion
                                 each species
                                 criteria       record and,
                                          were removed          therefore,
                                                           (Figure     1). Wesome    papers are
                                                                               then assessed    therepresented     more
                                                                                                    full text of the      thanlist
                                                                                                                      filtered   once   for the
                                                                                                                                    of articles
                                 species-specific
                                 to                analyses.
                                     identify records     that Wefit included    data oncriteria.
                                                                      our eligibility      the animal’s
                                                                                                    We captivity     status, whether
                                                                                                          only included                  it was
                                                                                                                              articles which
                                 free-living,anywhere
                                 described    captive (i.e.,
                                                          in contained
                                                              text, signsinside    a boarder such as
                                                                             of histopathological    orasuperficial
                                                                                                          zoo or wildlife   park oraffecting
                                                                                                                       dermatitis     reserve),
                                 or laboratory
                                 the  mammal in  (i.e., a wild To
                                                    question.    species
                                                                      ensureto comprehensiveness
                                                                               be used for laboratory       experiments).
                                                                                                        of the                 To determine
                                                                                                                literature search,     we also
                                 the total number
                                 screened            of dermatitis
                                            the bibliographies      and cases,  for each
                                                                          reference   listspaper, we split
                                                                                            from the  final the  data by
                                                                                                             full-text     species
                                                                                                                        articles     reported
                                                                                                                                 (Figure    1).
                                 (n = 244 individual species cases of dermatitis), then by the cause of dermatitis (n = 253
Animals 2021, 11, 1691                                                                                            5 of 19

                         differential cases of dermatitis), and, finally, by the individual mammals’ captivity status
                         (n = 257 cases). We also recorded the diagnosed type of dermatitis for each species in the
                         article (e.g., exudative dermatitis, ulcerative dermatitis) as well as whether the dermatitis
                         had a definitive causal agent identified (e.g., virus, bacteria, fungus, ectoparasite). If the
                         causal agent of the dermatitis was not found, we classed the cause as ‘unknown’.
                               The country for each dermatitis case was documented and each was aggregated
                         into their corresponding biogeographic realms (also known as ecozones). The World
                         Wildlife Fund classification of biogeographical realms [32,33] has eight ecozones, being
                         the broadest biogeographic division of all terrestrial ecosystems on Earth. These are
                         delineated by broad geographical features, such as oceans and mountain ranges which
                         have, over time, segregated evolving organisms. Therefore, biogeographic realms are based
                         on zoogeography evolutionary histories, ecoregions, and phytogeography, among many
                         other classification systems [33].
                               Species were updated to their current scientific name if it changed since the article was
                         published (e.g., Thalarctos maritimus to Ursus maritimus), or, if a subspecies was recorded, we
                         aggregated under the species name. We grouped species to higher taxa for further analyses
                         based on the types of dermatitis affecting similar wildlife, as follows: Artiodactyla, even-
                         toed ungulates (24 species); we split Carnivora into two groups, semi-aquatic Carnivora
                         (represented by five species of sea lions and seals from the family Otariidae and Phocidae),
                         and terrestrial Carnivora (20 species including felids, canids, and ursids); Diprotodontia,
                         marsupial mammals (14 species); Primates, non-human eutherian mammals (nine species);
                         and Rodentia, rodents (11 species). Five other orders had 10 or less dermatitis diagnoses
                         and fewer than five species within the grouping. Their individual syntheses are produced in
                         supplementary tables (Table S3): Didelphimorphia, represented by two species of opossum;
                         Eulipotyphla, represented by four species of hedgehog; Lagomorpha, hare and rabbit (four
                         species); Perissodactyla, rhinoceros (three species); Chiroptera, represented by four species
                         of bat from the family Vespertilionidae. Finally, four unique species did not belong to any
                         former (broader) order noted above: Elephas maximus (Asian elephant), Ornithorhynchus
                         anatinus (platypus), Procavia capensis (rock hyrax), and Zaedyus pichiy (pichi) (Table S3).
                               We used the International Union for Conservation of Nature’s Red List (hereafter
                         IUCN) (2021) to rank each species via their threat level [34]: Not Evaluated, Data Deficient,
                         Least Concern, Near Threatened, Vulnerable, Endangered, Critically Endangered, Extinct
                         in the Wild and Extinct. We also used this as a tool to rank the species with reported
                         dermatitis cases by global conservation status.

                         3. Overall Causes, Captivity Status, and Geographic Spread of Reported Dermatitis
                              Dermatitis in wildlife was reported in 216 papers (1925–2021), totaling 257 dermatitis
                         cases reported for terrestrial and semi-aquatic wildlife mammals (Table S2). There were 17
                         definitive causes (and another group for unknown) of dermatitis in wildlife, representing
                         76.4% of all cases (Table 2). The highest single proportion of dermatitis cases were of an
                         unknown cause (23.7%, n = 61), followed closely by mites (21.4%, n = 55) and then both
                         bacteria (16.3%, n = 42) and viruses (16.3%, n = 42) (Table 2). Mites as the causative agent
                         were found across the highest number of unique wildlife species (34 species), followed by
                         bacteria (29 species) and then both viruses and fugus (15 species) (Table 2).
                              Dermatitis was reported in 108 different mammal species, totaling 4118 individuals.
                         Wild, free-living mammals had a higher frequency of reported dermatitis cases (57.2%,
                         n = 147, 69 species), compared to wild animals that were brought into or born in captivity
                         (33.07%, n = 85, 51 species), and those under laboratory conditions (9.73%, n = 25, 12 species)
                         (Figure 2). The highest proportion of reported cases of dermatitis for free-living wildlife
                         was caused by mites (Figure 2). By contrast, unknown causes of dermatitis in captive
                         wildlife had the highest proportion of cases. Interestingly, wildlife from a laboratory setting
                         had no ‘other’ causes, and the primary cause of dermatitis was unknown (Figure 2).
Animals 2021, 11, 1691                                                                                                              6 of 19

                                   Table 2. Overall proportion of causes of dermatitis in terrestrial and semi-aquatic mammalian wildlife.
                                   This shows the cause of dermatitis, the diagnosis proportion (% out of 257 cases), the number of
                                   unique species per cause, and the number of ecozones for which the cause of dermatitis was reported
                                   in. For further analysis, causes with ‘*’ were combined into ‘Other’ category.

                                                                     Percentage Definitive           Species per
                                               Cause                                                                        Ecozone
                                                                         Diagnosis (n)                 Cause
                                         Apicomplexan *                    1.2% (3)                    2                   1
                                              Bacteria                   16.3% (42)                    29                  6
                                       Bacteria & Fungus *                 0.8% (2)                    1                   1
                                             Diptera *                     1.2% (3)                     3                  2
                                    Ectoparasite (unknown) *               0.4% (1)                    1                   1
Animals 2021, 11, x                            Fleas                       0.8% (2)                     2                  1 7 of 20
                                              Fungus                      9.0% (23)                    15                  3
                                              Louse *                      0.8% (2)                     2                  2
                                       Mineral deficiency *                0.4% (1)                     1                  1
                                       Dermatitis
                                               Mite was reported in 10821.4%
                                                                           different
                                                                                (55) mammal species,   34totaling 4118 individuals.
                                                                                                                           5
                                  Wild, Mite
                                         free-living
                                               & Fungusmammals
                                                         *       had a higher
                                                                           0.4% frequency
                                                                                (1)         of reported1dermatitis cases (57.2%,
                                                                                                                           1       n
                                  = 147,Mite
                                         69 species),
                                             & Nematode compared
                                                           *       to wild0.4%
                                                                            animals
                                                                                (1) that were brought   1 into or born in captivity
                                                                                                                           1
                                  (33.07%, Nematode
                                             n = 85, 51 species), and those2.7% under
                                                                                (7)                    6
                                                                                        laboratory conditions   (9.73%, n 2= 25, 12
                                              Plant  *                     1.6% (4)                     4                  2
                                  species) (Figure 2). The highest proportion of reported cases of dermatitis for free-living
                                            Protozoa *                     0.4% (1)                     1                  1
                                  wildlife was caused by mites (Figure 2). By contrast, unknown causes of dermatitis              in
                                                Tick                       2.3% (6)                    6                   2
                                  captive wildlife
                                             Unknown   had   the highest  proportion
                                                                         23.7% (61)     of  cases. Interestingly,
                                                                                                       35          wildlife5 from  a
                                  laboratory Virus
                                                setting had no ‘other’ 16.3%
                                                                           causes,
                                                                                (42) and  the  primary 15 cause of dermatitis
                                                                                                                           4    was
                                  unknown
                                  * Other. (Figure 2).

       Figure 2. Proportion of the top five causes of dermatitis reported in terrestrial mammalian wildlife, summarized into each
      Figure 2. Proportion of the top five causes of dermatitis reported in terrestrial mammalian wildlife, summarized into each
       captive or free-ranging group. Captivity status consists of wild free-living, wild-captive and wild-laboratory. The percentage
      captive or free-ranging group. Captivity status consists of wild free-living, wild-captive and wild-laboratory. The
       of definitive dermatitis causes reported in wildlife is shown for each group.
      percentage of definitive dermatitis causes reported in wildlife is shown for each group.
                                        The 257 wildlife dermatitis cases spanned six biogeographical realms (hereafter ‘eco-
                                       TheThe
                                   zone’).   257Nearctic
                                                 wildlifehad
                                                           dermatitis
                                                             the highestcases   spanned
                                                                           number          six biogeographical
                                                                                    of reported                     realms
                                                                                                  cases of dermatitis        (hereafter
                                                                                                                        (54.9%, n = 141,
                                  ‘ecozone’). The  Nearctic had   the highest   number   of  reported  cases  of dermatitis
                                   59 species), followed by Palearctic (29.2%, n = 75, 37 species), Australasia (9.3%,        (54.9%,  n
                                                                                                                                 n = 24,
                                  =18
                                    141, 59 species), followed  by  Palearctic  (29.2%,  n =  75, 37 species), Australasia   (9.3%,
                                      species), Neotropics (4.3%, n = 11, 9 species), Afrotropics (1.9%, n = 5, 4 species), and      n =
                                  24, 18 species), Neotropics  (4.3%, n  = 11, 9 species),
                                   Indomalaya (0.4%, n = 1, 1 species) (Figure 3).         Afrotropics   (1.9%,  n = 5, 4 species), and
                                  Indomalaya (0.4%, n = 1, 1 species) (Figure 3).
Animals2021,
Animals        11,x1691
         2021,11,                                                                                                                    87ofof2019

       Figure 3. The total number of reported dermatitis cases split into captivity status (wild free-living, wild captive and wild
      Figure 3. The total number of reported dermatitis cases split into captivity status (wild free-living, wild captive and wild
       laboratory), for five of the six biogeographical realms (ecozone) where mammalian wildlife dermatitis cases were reported in
      laboratory), for five of the six biogeographical realms  (ecozone) where mammalian wildlife dermatitis cases were reported
       the literature, with an ecozone area (million km2 ). There was one wild captive case recorded for the Indomalaya (7.5 m km2 )
      in the literature, with an ecozone area (million km2). There was one wild captive case recorded for the Indomalaya (7.5 m
       ecozone,
      km          which
          2) ecozone,    is not
                       which  is displayed.
                                 not displayed.

                                  4.4.Etiological
                                       EtiologicalAgents
                                                   AgentsResponsible
                                                            Responsiblefor forthe
                                                                               theCauses
                                                                                   CausesofofDermatitis
                                                                                               Dermatitisacross
                                                                                                             acrossMammalian
                                                                                                                    Mammalian
                                   Wildlife   Species
                                  Wildlife Species
                                          There were
                                         There  were over
                                                     over 6060causal agents
                                                                causal       of dermatitis
                                                                        agents              reported
                                                                                of dermatitis         in thein108
                                                                                                 reported         mammalian
                                                                                                                the           wildlife
                                                                                                                    108 mammalian
                                   species   (Table S4).  Due  to diagnostic   features,  identification  of  some  pathogens
                                  wildlife species (Table S4). Due to diagnostic features, identification of some pathogens    could
                                   only   be narrowed   to the family  or genus,  or in some   cases were   reported
                                  could only be narrowed to the family or genus, or in some cases were reported as an as an unknown
                                   agent (e.g., ‘unknown nematode’). The bacterial pathogen Dermatophilus congolensis had
                                  unknown agent (e.g., ‘unknown nematode’). The bacterial pathogen Dermatophilus
                                   caused dermatitis in the highest number of wildlife species (n = 18) and across the greatest
                                  congolensis had caused dermatitis in the highest number of wildlife species (n = 18) and
                                   number of wildlife orders (Table 3); followed by the Parapoxvirus genus (n = 13), and the
                                  across the greatest number of wildlife orders (Table 3); followed by the Parapoxvirus genus
                                   mite species Demodex and Notoedres, both causing dermatitis in eight species of wildlife
                                  (n = 13), and the mite species Demodex and Notoedres, both causing dermatitis in eight
                                   (Table 3). All other causal agents caused dermatitis in four or less species (Table S4).
                                  species of wildlife (Table 3). All other causal agents caused dermatitis in four or less
                                  species (Table S4).
                                   Table 3. The top seven causal agents of dermatitis in wildlife species, with all other causes effecting
                                   four or less species (Table S4). For each causal agent, the etiological category, the number of species
                                  Table 3. The top seven causal agents of dermatitis in wildlife species, with all other causes effecting
                                   the or
                                  four agent
                                          lesswas reported
                                              species (TabletoS4).
                                                               cause
                                                                   Fordermatitis in,agent,
                                                                       each causal   and the
                                                                                           thenumber   of orders
                                                                                               etiological       is shown.
                                                                                                           category,  the number of species
                                  the agent was reported to cause dermatitis in, and the number of orders is shown.
                                               Causal Agent                     Category           Species                  Orders
                                                 Causalcongolensis
                                         Dermatophilus    Agent                      Category
                                                                                Bacteria                 18Species           Orders
                                                                                                                              6
                                            Parapoxvirus (genus)
                                          Dermatophilus congolensis              Virus
                                                                                     Bacteria            13 18                26
                                            Demodex  sp. (genus)
                                             Parapoxvirus   (genus)              Mite Virus              8 13                 42
                                           Notoedres sp. (genus)                 Mite                     8                   3
                                             Demodex
                                              Sarcoptes sp. (genus)
                                                        scabiei                  Mite Mite               7    8               24
                                             Notoedres sp.
                                         Staphylococcus sp. (genus)
                                                            (genus)             BacteriaMite              7   8               63
                                           Malassezia sp. (genus)
                                                Sarcoptes  scabiei              FungusMite                6   7               22
                                          Staphylococcus sp. (genus)                 Bacteria                 7                 6
                                   5. CausesMalassezia   sp. (genus)
                                              of Dermatitis     across Wildlife OrdersFungus                  6                 2
                                        Artiodactyla had the highest number of dermatitis cases reported (n = 71, 27.6%,
                                   5 ecozones), with viruses being the greatest cause of dermatitis in this order (Figure 4a).
Animals 2021, 11, 1691                                                                                                                8 of 19

Animals 2021, 11, x                                                                                                                  9 of 20
                                     Semi-aquatic Carnivora had the lowest number of cases reported (n = 16; 6.2%; 2 ecozones),
                                     with fungus being their most common cause (Figure 4b). Terrestrial Carnivora was second
                                     highest (n = 59; 23.0%; 5 ecozones), with mite cases being most prevalent (Figure 4c).
                                    5. Causes of Dermatitis across Wildlife Orders
                                     Rodentia had 36 dermatitis cases reported (14.0%; 3 ecozones), with viruses being the
                                         Artiodactyla
                                     greatest            had the highest
                                              cause of dermatitis   in this number
                                                                            mammaloforder
                                                                                        dermatitis
                                                                                             (Figurecases    reported had
                                                                                                      4d). Primates     (n =2371,dermatitis
                                                                                                                                  27.6%, 5
                                    ecozones),   with (8.9%;
                                     cases reported    viruses4 ecozones),
                                                                being the greatest
                                                                             and thecause   of dermatitis
                                                                                      most prominent          in this
                                                                                                          causes      order (Figure
                                                                                                                   reported             4a).
                                                                                                                               were either
                                    Semi-aquatic    Carnivora    had   the  lowest  number     of  cases   reported    (n
                                     bacteria or unknown (Figure 4e). Diprotodontia had 19 dermatitis cases reported (7.4%;=  16;  6.2%;   2
                                    ecozones),   with fungus   being  their most  common
                                     2 ecozones), often with an unknown cause (Figure 4f).  cause   (Figure   4b). Terrestrial  Carnivora
                                    was second
                                          Primates highest
                                                     had the(nhighest
                                                               = 59; 23.0%;
                                                                      number5 ofecozones),  with
                                                                                  species and      mite
                                                                                               cases      cases being
                                                                                                      of dermatitis   formost    prevalent
                                                                                                                          wild laboratory
                                    (Figure  4c). Rodentia   had  36 dermatitis   cases reported   (14.0%;    3 ecozones),
                                     mammals (Figure 4e). Terrestrial Carnivora had the highest number (14) of unknown       with   viruses
                                    being  the greatest
                                     dermatitis   causes.cause  of dermatitis
                                                           Interestingly,      in this
                                                                           mites  havemammal
                                                                                        been shownorderto(Figure
                                                                                                            cause 4d).   Primates
                                                                                                                    dermatitis      had 23
                                                                                                                                 across   all
                                    dermatitis   cases
                                     orders except      reported (8.9%;
                                                     semi-aquatic         4 ecozones),
                                                                    Carnivora.   Bacteriaand
                                                                                          wasthe   most prominent
                                                                                               responsible               causescases
                                                                                                               for dermatitis     reported
                                                                                                                                       in all
                                    were
                                     orderseither
                                             exceptbacteria  or unknown
                                                     Diprotodontia,          (Figure reported
                                                                       with viruses   4e). Diprotodontia
                                                                                               as a cause ofhad     19 dermatitis
                                                                                                                dermatitis   in only cases
                                                                                                                                       three
                                    reported   (7.4%;
                                     (Figure 4).      2 ecozones),  often  with  an unknown    cause   (Figure   4f).

                             (a) Artiodactyla                                             (b) semi-aquatic Carnivora

                         (c) terrestrial Carnivora                                                 (d) Rodentia
                                                               Figure 4. Cont.
Animals
 Animals2021,
         2021,11,
               11,x1691                                                                                                                       10 9ofof2019

                              (e) Primates                                                            (f) Diprotodontia
                                         Wild Free-living          Wild Captive           Wild Laboratory

     Figure
      Figure4.4.The
                 Thecauses
                     causesofofdermatitis
                                dermatitisdiagnosed
                                           diagnosedforforeach
                                                           eachwildlife
                                                                wildlifeorder,
                                                                         order,and
                                                                                andfor
                                                                                    foreach
                                                                                        eachcaptivity
                                                                                             captivitystatus
                                                                                                       status(wild
                                                                                                              (wildfree-living,
                                                                                                                      free-living,wild
                                                                                                                                    wild
     captive,
      captive,and
               andwild
                    wildlaboratory),
                         laboratory),plotted
                                      plottedagainst
                                              againstthe
                                                      thenumber
                                                           numberofofdefinitive
                                                                      definitivedermatitis
                                                                                 dermatitisdiagnosis/cases:
                                                                                            diagnosis/cases:(a,c)
                                                                                                              (a,c)0–25
                                                                                                                    0–25cases;
                                                                                                                          cases;(b,d–e)
                                                                                                                                  (b,d–f)
     0–15
      0–15cases.
           cases.

                                       Primates had
                                  6. Threatened             the Reported
                                                        Species   highest number          of species and cases of dermatitis for wild
                                                                                with Dermatitis
                                laboratory       mammals       (Figure    4e).  Terrestrial
                                          Of the 108 wild mammal species reported              Carnivora
                                                                                                    as havinghaddermatitis,
                                                                                                                   the highest65.7%
                                                                                                                                  number  (n =(14)  of
                                                                                                                                                71) are
                                unknown
                                  regarded dermatitis         causes. Interestingly,
                                                as ‘Least Concern’        by the IUCN (2021)mites andhaveanother
                                                                                                            been shown
                                                                                                                    10.2% (n to =cause
                                                                                                                                   11) aredermatitis
                                                                                                                                             regarded
                                across
                                  as ‘Nearall orders     exceptThese
                                               threatened’.       semi-aquatic
                                                                         two groups  Carnivora.
                                                                                         have been  Bacteria  was by
                                                                                                        evaluated    responsible
                                                                                                                         the IUCNfor   as dermatitis
                                                                                                                                           species not
                                cases
                                  under  in immediate
                                             all orders except
                                                            threatDiprotodontia,
                                                                     of extinction and, withtherefore,
                                                                                               viruses reported      as a cause
                                                                                                            we omitted     these of82dermatitis
                                                                                                                                        species fromin
                                only    three   (Figure   4).
                                  further analysis on conservation concerns. We also omitted two species from the bat family
                                 Vespertilionidae, and one species of goral, Naemorhedus griseus, due to insufficient data
                                6.onThreatened
                                       their IUCN     Species   Reported
                                                        conservation          with(2.8%,
                                                                          status     Dermatitis
                                                                                            n = 3). The other 21.3% (n = 23) of species are
                                  classified
                                       Of theby   108IUCN
                                                        wildas   ‘Vulnerable’
                                                              mammal        species(12%,  n = 13),
                                                                                      reported     as‘Endangered’              n = 5) (n
                                                                                                                       (4.6%, 65.7%
                                                                                                       having dermatitis,               or ‘Critically
                                                                                                                                            = 71) are
                                  Endangered’         (4.6%,  n =  5) (Table    4). There   were   45  cases  of dermatitis
                                regarded as ‘Least Concern’ by the IUCN (2021) and another 10.2% (n = 11) are regarded         reported     across  the
                                  23  threatened       species: nine   cases   of  Critically  Endangered      (CR),
                                as ‘Near threatened’. These two groups have been evaluated by the IUCN as species not seven   cases  of   Endangered
                                 (EN), immediate
                                under      and 29 casesthreat
                                                            of Vulnerable      (VU) and,
                                                                   of extinction      (Tabletherefore,
                                                                                               3). There wewere   no species
                                                                                                               omitted    thesethat
                                                                                                                                  82 were
                                                                                                                                      speciesclassified
                                                                                                                                                 from
                                  as Extinct,
                                further           Extinct
                                             analysis    oninconservation
                                                               the Wild, or Regionally
                                                                                concerns. We   Extinct
                                                                                                    also reported
                                                                                                          omitted having      dermatitis.
                                                                                                                     two species      from the bat
                                familyTerrestrial        Carnivora
                                           Vespertilionidae,      andhad onethe    highest
                                                                              species        number
                                                                                        of goral,        of reported
                                                                                                     Naemorhedus        dermatitis
                                                                                                                     griseus,  due tocases    (n = 16),
                                                                                                                                         insufficient
                                  in  six   threatened     species,   followed      by  Artiodactyla       with  reported
                                data on their IUCN conservation status (2.8%, n = 3). The other 21.3% (n = 23) of species    cases   (n   = 9) in four
                                  threatened       species   (Table   4).   Dermatitis     cases   were    reported
                                are classified by IUCN as ‘Vulnerable’ (12%, n = 13), ‘Endangered’ (4.6%, n = 5) or    more   often    in  threatened
                                  species outside
                                ‘Critically              of their(4.6%,
                                                Endangered’        endemic n = 5)ecozone    and
                                                                                   (Table 4).     within
                                                                                                There       captivity
                                                                                                         were  45 cases(57.8%,    n = 26)reported
                                                                                                                          of dermatitis      (Table 4).
                                 There     was    no   consistent   cause    of dermatitis    identified    for the  45  cases
                                across the 23 threatened species: nine cases of Critically Endangered (CR), seven cases of      reported     across  all
                                  threatened      species   (Table  S5).   In threatened     species,   treatment   of
                                Endangered (EN), and 29 cases of Vulnerable (VU) (Table 3). There were no species that  dermatitis   was    attempted
                                  in 26classified
                                were       cases (58%),      which consisted
                                                        as Extinct,   Extinct inofthe  medical
                                                                                           Wild, intervention
                                                                                                    or RegionallyforExtinct
                                                                                                                         the cure   of the cause
                                                                                                                                 reported     havingof
                                  dermatitis
                                dermatitis.       (e.g., antibiotics;   ivermectin),     or for  mitigation   of  clinical signs   (e.g.,  removal   of
                                  lesions) if the cause was chronic (e.g., Feline Herpes Virus). Treatment was successful in
     Table 4. International Union most    instances (nof=Nature’s
                                   for Conservation          17) and(IUCN)
                                                                        was not     attempted
                                                                                  Red             in 19 cases
                                                                                       List of threatened   wild(42%)
                                                                                                                  mammal(Table  S5). reported
                                                                                                                             species
     as having dermatitis. The 23 species categorized as ‘Critically Endangered’ (CR), ‘Endangered’ (EN), and ‘Vulnerable’
     (VU) are shown, including their order and total number of cases. The number of dermatitis cases within endemic ecozones
     are shown for each species and the number of cases within non-endemic ecozones. Both ecozone categories are separated
     into the following captivity statuses of: Wild Captive (WC), Wild Free-living (WFL) and Wild Laboratory (WL). * WFL has
     one reported case within a non-endemic ecozone (*), and WL has no reported cases across non-endemic ecozones, so the
     columns have been removed to simplify the table.
                                                                                                                                   Non-Endemic
                                                 Threatened                                Total     Endemic Ecozone Cases
       IUCN (2021) Threatened Species                                   Order                                                     Ecozone Cases *
                                                  Category                                 Cases
                                                                                                     WFL       WC       WL             WC
Animals 2021, 11, 1691                                                                                                                      10 of 19

      Table 4. International Union for Conservation of Nature’s (IUCN) Red List of threatened wild mammal species reported as
      having dermatitis. The 23 species categorized as ‘Critically Endangered’ (CR), ‘Endangered’ (EN), and ‘Vulnerable’ (VU)
      are shown, including their order and total number of cases. The number of dermatitis cases within endemic ecozones are
      shown for each species and the number of cases within non-endemic ecozones. Both ecozone categories are separated
      into the following captivity statuses of: Wild Captive (WC), Wild Free-living (WFL) and Wild Laboratory (WL). * WFL has
      one reported case within a non-endemic ecozone (*), and WL has no reported cases across non-endemic ecozones, so the
      columns have been removed to simplify the table.

                                                                                                                                Non-Endemic
                                                         Threatened                                    Endemic Ecozone Cases
          IUCN (2021) Threatened Species                                    Order        Total Cases                           Ecozone Cases *
                                                          Category
                                                                                                       WFL     WC       WL          WC
                                                                          terrestrial
                 Canis rufus (red wolf)                     CR                               1                   1
                                                                          Carnivora
        Dasyprocta mexicana (Mexican agouti)                CR            Rodentia            1                  1
         Diceros bicornis (black rhinoceros)                CR          Perissodactyla        5         2                            3
                                                                          terrestrial
           Mustela lutreola (European Mink)                 CR                               1                                       1
                                                                          Carnivora
    Pongo pygmaeus pygmaeus (Northwest Bornean
                                                            CR            Primates            1                                      1
                    orangutan)
                                                                           terrestrial
              Ailurus fulgens (red panda)                   EN                               2                                       2
                                                                          Carnivora
                                                                             Other
          Elephas maximus (Asian Elephant)                  EN                               2                   1                   1
                                                                        (Elephantidae)
          Pentalagus furnessi (Amami rabbit)                EN           Lagomorpha          1          1
    Petrogale persephone (Proserpine rock wallaby)          EN          Diprotodontia        1          1
         Symphalangus syndactylus (siamang)                 EN              Primates         1                                       1
                                                                           terrestrial
              Acinonyx jubatus (cheetah)                    VU                               5                   1                   4
                                                                          Carnivora
     Alouatta palliata (Mantled Howler Monkey)              VU              Primates         1          1
       Budorcas taxicolor tibetana (Sichuan takin)          VU           Artiodactyla        1                                       1
    Hippopotamus amphibius (Nile hippopotamus)              VU           Artiodactyla        3                                       3
         Lagothrix lagotricha (woolly monkey)               VU              Primates         1                                       1
       Macaca fascicularis (crab-eating macaque)            VU              Primates         2                                       2*
    Petrogale penicillata (brush-tailed rock-wallaby)       VU          Diprotodontia        1          1
              Phascolarctos cinereus (koala)                VU          Diprotodontia        1          1
               Rangifer tarandus (caribou)                  VU           Artiodactyla        4          1        2       1
        Rhinoceros unicornis (Indian rhinoceros)            VU          Perissodactyla       2                                       2
                 Rusa unicolor (Sambar)                     VU           Artiodactyla        1                                       1
                                                                           terrestrial
           Tremarctos ornatus (Andean bear)                 VU                               3                                       3
                                                                          Carnivora
                                                                           terrestrial
             Ursus maritimus (polar bear)                   VU                               4          2        1                   1
                                                                          Carnivora
                                                                            Total            45         10       7       1         26(*1)

                                            7. Discussion
                                                 Overall, there were more than 60 causal agents of dermatitis reported in wildlife,
                                            showing that this clinical sign can manifest from a variety of causes. However, the highest
                                            single proportion of reported cases was of an unknown cause. This may be since identifying
                                            the causal agent is recognized as a key challenge in the literature, and there are a variety of
                                            sampling techniques needed to correctly detect the dermatitis agent. Of the 60 definitive
                                            causes of dermatitis, mites were the most common across all species. Bacteria were the
                                            second highest cause of dermatitis across wild mammalian species, and this was driven by
                                            Dermatophilus congolensis (causing dermatophilosis) infection. There were a higher number
                                            of cases reported in free-ranging wildlife, and captivity had a greater role to play for the
                                            development of dermatitis in IUCN threatened species. However, the causes of dermatitis
                                            are rarely reported as a conservation issue for threatened species. Reporting biases are
                                            recognized in the ecozone Nearctic and the mammalian orders of terrestrial Carnivora and
                                            Artiodactyla.

                                            7.1. The Main Causes of Dermatitis in Mammalian Wildlife: Mites, Bacteria and Viruses
                                                  Due to the wide taxonomic range of mites’ (such as Sarcoptes scabiei) host species,
                                            it is unsurprising that they account for the highest percentage of diagnosed dermatitis
                                            cases in the greatest number of wildlife species [35–37]. Mites were the predominant
                                            cause of dermatitis reports in five of the six mammal orders, and, across these, over
                                            15 genera of mites were represented with the top three: Demodex sp., Notoedres sp. and
                                            Sarcoptes scabiei. Demodex mites are commensal, found in hair follicles across an array
Animals 2021, 11, 1691                                                                                            11 of 19

                         of taxa, including humans. However, under favorable environments, they can become
                         opportunistic and an over proliferation can cause the skin condition demodicosis, which
                         can cause dermatitis [38]. Conversely, the Notoedres sp. and Sarcoptes scabiei are both from
                         the Sarcoptidae family, and are highly contagious pathogens that can infest a wide variety
                         of animal orders [35–37]. Notoedres sp. can cause notoedric mange, and is associated with
                         the development of dermatitis, particularly in rodents and felids, which was supported by
                         the findings in our review [37]. In fact, both mites can cause an array of dermatological
                         signs, from alopecia, inflammation, to even secondary infections and death. S. scabiei causes
                         sarcoptic mange and is an emerging infectious disease for some species, exerting animal
                         welfare and conservation pressures [35,36]. However, given the wide host range of this
                         mite species, it was surprising this mite was not the leading causal agent in our review.
                         This may be because dermatitis is not a representative clinical sign of mange, or clinical
                         signs were not specifically mentioned in S. scabiei studies.
                               Given their global ubiquity and wide host range, it was unsurprising that viruses and
                         bacteria were the second highest causative agents of dermatitis cases [39,40]. Viruses were
                         mostly represented by the Parapoxvirus (genus), in Artiodactyla and Rodentia. High report-
                         ing of this cause may be since the Parapoxvirus is found worldwide and can be transmitted
                         between domestic mammals and wildlife in the Artiodactyla order [41]. The most common
                         bacteria species was Dermatophilus congolensis and bacteria from the genus Staphylococcus.
                         Some bacteria, such as Staphylococcus sp., are a part of normal skin microflora, and certain
                         host and environmental factors may cause these commensal bacteria to become problem-
                         atic and cause skin conditions, such as atopic dermatitis [42]. Dermatophilus congolensis
                         (causing dermatophilosis) bacterium caused dermatitis across the most species; these bac-
                         teria are found globally, have a wide host range, and the epidemiology is broadly known
                         in the literature [24,39,43]. Dermatophilosis has caused dermatitis in species as diverse
                         as the meadow jumping mouse (Zapus hudsonius) [29] and ground squirrels (Urocitellus
                         columbianus columbianus) [44] from the order Rodentia; owl monkey (Aotus trivirgatus) [45]
                         and orangutans (Pongo pygmaeus pygmaeus) [26] from Primates; polar bears (Ursus mar-
                         itimus) [46] and racoons (Procyon lotor) [47] from terrestrial Carnivora; and white-tail deer
                         (Odocoileus virginianus) [48] from Artiodactyla, to name a few.

                         7.2. Captivity Status and Dermatitis in Wild Mammals
                               Dermatitis was reported to occur in wild free-living mammals more often than their
                         wild laboratory or captive counterparts. This may be due to under reporting of dermatitis
                         in captive wildlife, treatment regimens for wildlife in captivity, or biases towards the report-
                         ing of free-living individuals. Dermatological problems are common in captive wildlife,
                         ranging from secondary infection due to poor husbandry to self-inflicted lesions subse-
                         quent to stereotypic behaviour [49,50]. Therefore, it is possible due to their commonality,
                         skin problems are treated without being reported in the literature; and skin issues in wild
                         animals are deemed more important. Furthermore, dermatological issues in wild captive
                         animals may be treated before the signs of disease become advanced enough to warrant
                         reporting, since individuals within captivity or laboratory settings are often quarantined
                         and treated for common diseases as a precaution and are subject to routine examinations
                         for signs of disease [51,52], whereas free-living individuals may be more likely to show
                         later stages of dermatitis clinical signs since early treatment is unlikely.
                               Wild free-living mammals may be more likely to be reported with dermatitis or show
                         later stages of clinical signs since: (i) there are no preventative steps in stopping spread
                         and limited veterinary intervention; (ii) they come into contact with many more species
                         and individuals which might have pathogen causing dermatitis (such as other mammals,
                         domestic animals and livestock) [53]; and (iii) they have unregulated environmental factors,
                         which vary from contact with unusual plants [54] to opportunistic pathogens [55].
                               Primates had the highest reported cases of dermatitis for wild laboratory, owing
                         to their regular use as an experimental subject. For wild laboratory mammals, where
                         almost half of the dermatitis causes were ‘unknown’, it is likely that commensal and
Animals 2021, 11, 1691                                                                                            12 of 19

                         non-pathogenic parasites were a prevailing problem, due to stress associated with an
                         unnatural, confined environment [51]. In fact, such speculation was made for both captive
                         and laboratory animals in Van Horn et al. [56] and Steinmetz et al. [6] where unknown
                         dermatitis was presumed psychogenic of origin.

                         7.3. Threatened Species with Dermatitis
                               Generally, reported cases of dermatitis in the literature largely described the occurrence
                         of dermatitis in the species, or in a particular part of a species’ range, for the first time.
                         There were few reports of dermatitis being a primary concern for the conservation of a
                         species, despite our identification of 23 threatened species reported as having dermatitis.
                         The causes of dermatological lesions reduce fitness and thus constitute another pressure on
                         threatened populations, with many species driven to extinction often due to compounding
                         anthropogenic activities [57]. However, many threatened species’ articles only briefly
                         mentioned causes of dermatitis as a conservation concern or that the mammal is endangered
                         (e.g., [5,46,58]). Reports which focused on dermatitis causes as a conservation threat
                         for a species, for example Munson et al. [5], Witte et al. [59] and Van Horn et al. [56],
                         discussed dermatitis induced health problems and mortality could affect captive population
                         sustainability and husbandry management. However, overall, there was no pattern in
                         reporting treatment success or failure for threatened species. Pathogens causing dermatitis
                         were also identified as a conservation threat to the red squirrel (Sciurus vulgaris), San
                         Joaquin Kit Fox (Vulpes macrotis mutica), and Amargosa vole (Microtus californicus scirpensis)
                         despite these mammals not being identified by the IUCN as at-risk species [21,23,60,61].
                         Therefore, it is important to consider that (1) some mammals may not have been classified as
                         threatened when dermatitis was reported in the past, and (2) some species and subspecies
                         may be missed by the IUCN and, as the classification is updated, more species may be
                         added to the threatened categories in the future.
                               The threatened species cases in our review show that 33 dermatitis cases (total of 45)
                         were in captivity. This may be due to the routine observations for captive individuals,
                         compared to their free-living counterparts. However, we determine that there may be
                         multiple compounding factors which may cause threatened species in captivity to be more
                         likely to exhibit dermatitis, such as: lack of genetic diversity, added psychological stress
                         in captivity [56,62], exposure to alien pathogens, and environmental exacerbations [63].
                         Loss of genetic diversity is common in many threatened species, potentially lowering
                         their resistance to diseases and inflammatory conditions, making them more prone to
                         agents which can cause dermatitis [64–66]. Loss of genetic diversity may be one of the
                         reasons terrestrial Carnivora had the highest number of threatened species dermatitis cases
                         reported, because many lack the genetic diversity of other mammals [65,67]. Low genetic
                         diversity and small population size are also a conservation concern, particularly for the
                         management of breeding programs, and act in synergy with disease and a species’ capacity
                         to adapt to changing environmental conditions [64,66,68,69]. Conversely, large populations
                         of nonthreatened individuals have a greater ability to adapt to captivity stressors [63].
                               Physiological responses to stress, or stress induced by environmental changes, might also
                         manifest as dermatitis in threatened species in captivity via immune suppression [62,63,67].
                         For example, Munson et al. [65] describe both captive and free-ranging cheetahs having
                         the same genetic diversity; however, captive cheetahs had worse reactions to viral infec-
                         tions and severe inflammatory reactions to common infections, suggesting that the local
                         environment is important in determining health trajectories of individuals, beyond just
                         genetic susceptibility. Additionally, since the majority (70%) of dermatitis cases for captive
                         threatened species were located outside of their endemic range; captive stressors may be
                         exacerbated for threatened species due to exposure to alien pathogens and sub-optimal
                         environmental conditions [69–71]. It is well known that the introduction of wild non-native
                         species to foreign geographic ranges has increased potential for disease emergence and
                         outbreaks [71,72].
Animals 2021, 11, 1691                                                                                           13 of 19

                               For several species, the development of dermatitis as a reaction to disease is associated
                         with genetic and behavioral features [73–75]. This is particularly true of rhinoceroses,
                         which are especially prone to skin diseases and lesions [5]. Dermatitis manifestation
                         in rhinoceroses was not due to one specific bacterial or viral infection, but was instead
                         associated with concurrent diseases or events, where dermal erosions or ulcers are the
                         first clinical signs of underlying health issues [5,76]. Determining the reasons why some
                         threatened species may be more susceptible to dermatological diseases can help inform
                         management practices and husbandry behaviors within captivity.

                         7.4. Reporting Bias for Orders of Mammalian Wildlife and across Ecozones
                               Our synthesis might be impacted by a reporting bias for dermatitis in the mammalian
                         orders of Artiodactyla and terrestrial Carnivora. These orders have similar and lower
                         number of species, at about 220 and 268, respectively, compared to Primates (300) and
                         Rodentia (1500). We suspect that, with a higher number of species, there is a greater chance
                         of dermatitis occurring and being opportunistically observed in that mammalian order.
                         Potential observation bias for reporting dermatitis in larger animals may be related to
                         chance occurrence, since dermatitis is easier to see in larger animals [77,78] or reported
                         due to relative-attention bias [79]. Furthermore, it is known that historical biodiversity
                         records for charismatic species, particularly large mammals, have reporting biases [80,81].
                         This may also explain the high number of reported dermatitis cases in both terrestrial
                         Carnivora and Artiodactyla, and less for Rodentia, despite the order Rodentia having about
                         six-fold more species. Additionally, Artiodactyla species are genetically similar (or, in some
                         cases, used as) agricultural animals [82,83], or game species [48]. Clegg et al. [84] reported
                         dermatitis for the first time in wild elk; elk potentially contracted the bacterial species
                         Treponema from livestock pastures and could now be a reservoir for domestic livestock and
                         other wild animals. This is especially the case of the genus Parapoxvirus, with articles on
                         this dermatitis causing agent focusing on domestic livestock species or human infections
                         from wildlife [41,85]. This implies that Artiodactyla species’ proximity to humans and
                         the potential for economic consequences might also explain why this order is the primary
                         focus of dermatitis reports.
                               Biogeographic realms have been used as the broadest scale for identifying and plan-
                         ning the conservation of species [86,87] and biotic processes [88,89]. However, applying
                         macroecological generalities to complex systems such as infectious disease has been viewed
                         as an unresolved challenge and, until recently, biogeography has rarely been included
                         in management of human or veterinary health [90,91]. For certain dermatitis causes, an
                         ecozone’s environmental attributes could inhibit or exacerbate dermatitis severity, spread
                         of causes and growth of lesions. Therefore, there is no doubt that biogeographical analysis
                         offers a potentially important explanatory role that can provide insight into spatial pat-
                         terns of multiple systems [90,92]. However, our synthesis on the literature to date suggest
                         that funding and economics play a greater role in the reporting of dermatitis in ecozones.
                         Indeed, our overview of this research suggests that opportunistic reports have led to an
                         artificial trend of dermatitis in the Nearctic [79,93]. For example, dermatophilosis is more
                         likely to occur in relatively low altitude areas with tropical and subtropical climates [39].
                         Therefore, in theory, dermatophilosis would be more likely to be reported in the Afrotropic
                         and Neotropic ecozones [26]; however, more cases of dermatophilosis were reported within
                         the Nearctic. Geographical bias in reporting has been found in other studies [94–96],
                         supporting the potential for a skew towards reports in the Nearctic ecozone.

                         7.5. Limitations of Reviewing Clinical Signs of Diseases or Irritants
                             Our review provides a valuable synthesis of the use of the term dermatitis and patterns
                         in mammalian wildlife. Indeed, such syntheses on common causes of dermatitis have
                         been produced for domestic and livestock animals [97,98]; however, in wildlife, focus has
                         been primarily on either (i) a certain type of agent affecting the wildlife, e.g., parapoxvirus
                         or Neospora caninum infection in wildlife (e.g., [41,99,100]) or (ii) on pathogens affecting
Animals 2021, 11, 1691                                                                                              14 of 19

                          individual species (e.g., captive pinnipeds) which are, by chance, or perhaps due to visual
                          dermatological conditions (e.g., [18,59,101]). Our unique synthesis, while not completely
                          exhaustive, is representative of published information across different mammalian wildlife
                          groups for a clinical sign (dermatitis), which has, to date, been overlooked but is important
                          to consider.
                                However, we have identified several limitations in reviewing clinical signs of pathogen
                          agents. Firstly, the variable use of clinical signs in diseases or irritants is a key challenge in
                          undertaking syntheses. For example, histopathological descriptions of dermatitis may be
                          used without applying the term explicitly. Due to this, the search term for dermatitis could
                          underestimate the number of articles with dermatitis, since it does not capture cases with
                         ‘dermatitis like’ clinical signs.
                                Furthermore, the term dermatitis may not be used in the title, abstract or key words
                          because it is: (i) not a key feature of the histopathology of that pathogen; (ii) unclearly
                          defined, such as a dermatitis like term; or (iii) the clinical signs are not mentioned at all,
                          most likely because it is a well-known pathogen. The latter may be the case for Sarcoptic
                          mange, caused by the mite Sarcoptes scabiei in over 100 mammalian species. However, we
                          only found S. scabiei as the cause of dermatitis in seven wildlife species in our review, and,
                          therefore, dermatitis is either not a term used for normally describing mange, or, because it
                          is a well-known pathogen, the histological signs are not described in the abstract. In another
                          example, White Nose Syndrome (WNS) in bats has been described as having histologically
                          identifiable infiltrative fungal dermatitis [22]. However, we had no articles with WNS in
                          our synthesis. Two articles in our review were screening for WNS in bats; however, they
                          describe dermatitis as the main clinical signs of other pathogen infections [55,102].
                                Conversely, the clinical signs of disease would be more likely to be within the title
                          and abstract if the clinical sign in question is unknown, since the dermatological origin
                          is not identified. To combat this, we suggest that the clinical aspects of the skin diseases
                          and irritation be described in the abstract of papers, regardless of whether the pathogen
                          is well known. Despite limitations of reporting of clinical signs of skin diseases and
                          irritants, our synthesis identifies the overall causes and patterns of dermatitis in wild
                          mammalian species.

                         8. Conclusions
                               This review has identified that, overall, there seems to be bias towards reporting
                         dermatitis cases when the cause is unknown or when presented in a species for the first time.
                         For some species, it was noted that the underlying causal agents were first investigated due
                         to the visibility of dermal lesions (e.g., [5,78]). Through the valuable compendium of reports,
                         we have additionally identified that, when the causal agent of dermatitis is unknown,
                         reports may be more likely to include dermatitis within the title and abstract (since the
                         dermatological symptoms are in question and the origin not identified). Furthermore,
                         the search term for dermatitis could also underestimate the number of articles and cases
                         showing dermatitis, since the term might not be included in the title or abstract of articles
                         dealing with a disease or agent for which dermatitis is usually just one of several possible
                         manifestations. Conversely, for threatened species with dermatitis, 15 cases from 45 were of
                         unknown causes (Table S5). This is perhaps because the identification of unknown causes
                         of dermatitis, and the successful treatment of dermatitis lesions, regardless of cause, are of
                         particular interest to threatened species given their parlous conservation status.
                               In general, dermatitis is rarely reported as a conservation issue; however, we have
                         discovered that some threatened species may be more likely to exhibit dermatitis in cap-
                         tivity, and, for others, diseases often manifest, at least in part, as dermatitis. This review
                         highlights that, in some cases, species of concern are declining due to specific reasons that
                         are clinically revealed as dermatitis. However, dermatitis reporting in wild semi-aquatic
                         and terrestrial mammals remains subject to many biases. As such, future case studies of
                         diseases should: (i) document the main clinical signs and manifestations of the disease or
                         causative agent in the abstract of reports, and (ii) encompass a range of dermatological
Animals 2021, 11, 1691                                                                                                              15 of 19

                                   conditions, since an animal may be suffering a form of dermatitis but was classified as
                                   another skin disorder (e.g., dermatophilosis). With our suggestions, we can bridge cross-
                                   disciplinary gaps between veterinary, genetics, captive management, and conservation,
                                   and further research can determine common spatial patterns of dermatological diseases for
                                   wild mammals.

                                   Supplementary Materials: The following are available online at https://www.mdpi.com/article/
                                   10.3390/ani11061691/s1, Search terms S1: The search terms used to identify the relevant literature
                                   in each database, Table S2: Complete dataset of all 216 articles that reported wildlife dermatitis,
                                   Table S3: All individually reported dermatitis cases for each order not presented in the synthesis,
                                   Table S4: Etiological agents responsible for the causes of dermatitis across mammalian wildlife
                                   species, Table S5: Each reported threatened species dermatitis cases and their corresponding IUCN
                                   (2021) threatened categories, concurrent disease, dermatitis treatment, and whether the treatment
                                   resolved dermatitis.
                                   Author Contributions: Conceptualization, E.M.R., B.W.B., S.C. and J.C.B.; methodology and formal
                                   analysis, E.M.R. and J.C.B.; data curation, E.M.R.; writing—original draft preparation, E.M.R.;
                                   writing—review and editing, E.M.R., B.W.B., S.C. and J.C.B.; supervision, B.W.B., S.C. and J.C.B.;
                                   funding acquisition, B.W.B. and S.C. All authors have read and agreed to the published version of
                                   the manuscript.
                                   Funding: This research was funded by the Australian Research Council, Grant Nos. FL160100101
                                   and LP180101251, and the University of Tasmania CoSE Research Training Program.
                                   Institutional Review Board Statement: Not applicable.
                                   Data Availability Statement: The data presented in this study are available in the Supplementary
                                   Materials section.
                                   Conflicts of Interest: The authors declare no conflict of interest.

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